Circadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.

Multinucleate cells occur in every biosphere and across the kingdoms of life, including in the human body as muscle cells and bone-forming cells. Data from filamentous fungi suggest that, even when bathed in a common cytoplasm, nuclei are capable of autonomous behaviors, including division. How does...

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Autores principales:	Leif Zinn-Brooks, Marcus L Roper
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/4f425e3f0c3141cb95ebda760729eec3
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spelling	oai:doaj.org-article:4f425e3f0c3141cb95ebda760729eec32021-12-02T19:58:09ZCircadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.1553-734X1553-735810.1371/journal.pcbi.1008828https://doaj.org/article/4f425e3f0c3141cb95ebda760729eec32021-08-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1008828https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Multinucleate cells occur in every biosphere and across the kingdoms of life, including in the human body as muscle cells and bone-forming cells. Data from filamentous fungi suggest that, even when bathed in a common cytoplasm, nuclei are capable of autonomous behaviors, including division. How does this potential for autonomy affect the organization of cellular processes between nuclei? Here we analyze a simplified model of circadian rhythm, a form of cellular oscillator, in a mathematical model of the filamentous fungus Neurospora crassa. Our results highlight a potential role played by mRNA-protein phase separation to keep mRNAs close to the nuclei from which they originate, while allowing proteins to diffuse freely between nuclei. Our modeling shows that syncytism allows for extreme mRNA efficiency-we demonstrate assembly of a robust oscillator with a transcription rate a thousand-fold less than in comparable uninucleate cells. We also show self-organized division of the labor of mRNA production, with one nucleus in a two-nucleus syncytium producing at least twice as many mRNAs as the other in 30% of cycles. This division can occur spontaneously, but division of labor can also be controlled by regulating the amount of cytoplasmic volume available to each nucleus. Taken together, our results show the intriguing richness and potential for emergent organization among nuclei in multinucleate cells. They also highlight the role of previously studied mechanisms of cellular organization, including nuclear space control and localization of mRNAs through RNA-protein phase separation, in regulating nuclear coordination.Leif Zinn-BrooksMarcus L RoperPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 8, p e1008828 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Leif Zinn-Brooks Marcus L Roper Circadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.
description	Multinucleate cells occur in every biosphere and across the kingdoms of life, including in the human body as muscle cells and bone-forming cells. Data from filamentous fungi suggest that, even when bathed in a common cytoplasm, nuclei are capable of autonomous behaviors, including division. How does this potential for autonomy affect the organization of cellular processes between nuclei? Here we analyze a simplified model of circadian rhythm, a form of cellular oscillator, in a mathematical model of the filamentous fungus Neurospora crassa. Our results highlight a potential role played by mRNA-protein phase separation to keep mRNAs close to the nuclei from which they originate, while allowing proteins to diffuse freely between nuclei. Our modeling shows that syncytism allows for extreme mRNA efficiency-we demonstrate assembly of a robust oscillator with a transcription rate a thousand-fold less than in comparable uninucleate cells. We also show self-organized division of the labor of mRNA production, with one nucleus in a two-nucleus syncytium producing at least twice as many mRNAs as the other in 30% of cycles. This division can occur spontaneously, but division of labor can also be controlled by regulating the amount of cytoplasmic volume available to each nucleus. Taken together, our results show the intriguing richness and potential for emergent organization among nuclei in multinucleate cells. They also highlight the role of previously studied mechanisms of cellular organization, including nuclear space control and localization of mRNAs through RNA-protein phase separation, in regulating nuclear coordination.
format	article
author	Leif Zinn-Brooks Marcus L Roper
author_facet	Leif Zinn-Brooks Marcus L Roper
author_sort	Leif Zinn-Brooks
title	Circadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.
title_short	Circadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.
title_full	Circadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.
title_fullStr	Circadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.
title_full_unstemmed	Circadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.
title_sort	circadian rhythm shows potential for mrna efficiency and self-organized division of labor in multinucleate cells.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/4f425e3f0c3141cb95ebda760729eec3
work_keys_str_mv	AT leifzinnbrooks circadianrhythmshowspotentialformrnaefficiencyandselforganizeddivisionoflaborinmultinucleatecells AT marcuslroper circadianrhythmshowspotentialformrnaefficiencyandselforganizeddivisionoflaborinmultinucleatecells
_version_	1718375776587350016

Circadian rhythm shows potential for mRNA efficiency and self-organized division of labor in multinucleate cells.

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